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L-arginine and N-carbamoylglutamic acid supplementation enhance young rabbit growth and immunity by regulating intestinal microbial community

  • Sun, Xiaoming (Laboratory Animal Center, College of Animal Science, Jilin University) ;
  • Shen, Jinglin (Laboratory Animal Center, College of Animal Science, Jilin University) ;
  • Liu, Chang (School of Grains, Jilin Business and Technology College) ;
  • Li, Sheng (Laboratory Animal Center, College of Animal Science, Jilin University) ;
  • Peng, Yanxia (Laboratory Animal Center, College of Animal Science, Jilin University) ;
  • Chen, Chengzhen (Laboratory Animal Center, College of Animal Science, Jilin University) ;
  • Yuan, Bao (Laboratory Animal Center, College of Animal Science, Jilin University) ;
  • Gao, Yan (Laboratory Animal Center, College of Animal Science, Jilin University) ;
  • Meng, Xianmei (School of Grains, Jilin Business and Technology College) ;
  • Jiang, Hao (Laboratory Animal Center, College of Animal Science, Jilin University) ;
  • Zhang, Jiabao (Laboratory Animal Center, College of Animal Science, Jilin University)
  • Received : 2018.12.26
  • Accepted : 2019.05.21
  • Published : 2020.01.01

Abstract

Objective: An experiment was conducted to determine the effects of L-arginine (L-Arg) and N-carbamoylglutamic acid (NCG) on the growth, metabolism, immunity and community of cecal bacterial flora of weanling and young rabbits. Methods: Eighteen normal-grade male weanling Japanese White rabbits (JWR) were selected and randomly divided into 6 groups with or without L-Arg and NCG supplementation. The whole feeding process was divided into weanling stage (day 37 to 65) and young stage (day 66 to 85). The effects of L-Arg and NCG on the growth, metabolism, immunity and development of the ileum and jejunum were compared via nutrient metabolism experiments and histological assessment. The different communities of cecal bacterial flora affected by L-Arg and NCG were assessed using high-throughput sequencing technology and bioinformatics analysis. Results: The addition of L-Arg and NCG enhanced the growth of weanling and young rabbit by increasing the nitrogen metabolism, protein efficiency ratio, and biological value, as well as feed intake and daily weight gain. Both L-Arg and NCG increased the concentration of immunoglobulin A (IgA), IgM, and IgG. NCG was superior to L-Arg in promoting intestinal villus development by increasing villus height, villus height/crypt depth index, and reducing the crypt depth. The effects of L-Arg and NCG on the cecal bacterial flora were mainly concentrated in different genera, including Parabacteroides, Roseburia, dgA-11_gut_group, Alistipes, Bacteroides, and Ruminococcaceae_UCG-005. These bacteria function mainly in amino acid transport and metabolism, energy production and conversion, lipid transport and metabolism, recombination and repair, cell cycle control, cell division, and cell motility. Conclusion: L-Arg and NCG can promote the growth and immunity of weanling and young JWR, as well as effecting the jejunum and ileum villi. L-Arg and NCG have different effects in the promotion of nutrient utilization, relieving inflammation and enhancing adaptability through regulating microbial community.

Acknowledgement

Supported by : Jilin Province

References

  1. Fortun-Lamothe L, Boullier S. A review on the interactions between gut microflora and digestive mucosal immunity. Possible ways to improve the health of rabbits. Livest Sci 2007;107:1-18. https://doi.org/10.1016/j.livsci.2006.09.005 https://doi.org/10.1016/j.livsci.2006.09.005
  2. Padilha M, Licois D, Coudert P. Frequency of the carriage and enumeration of Escherichia coli in caecal content of 15 to 49 day old rabbits. Proceedings 6th World Rabbit Congress, 1996 July 9-12; Toulouse, France.
  3. Michelland R, Combes S, Monteils V, Cauquil L, Gidenne T, Fortun-Lamothe L. Rapid adaptation of the bacterial community in the growing rabbit caecum after a change in dietary fibre supply. Animal 2011;5:1761-8. https://doi.org/10.1017/S1751731111001005 https://doi.org/10.1017/S1751731111001005
  4. Hugenholtz P, Hooper SD, Kyrpides NC. Focus: synergistetes. Environ Microbiol 2009;11:1327-9. https://doi.org/10.1111/j.1462-2920.2009.01949.x https://doi.org/10.1111/j.1462-2920.2009.01949.x
  5. Penders J, Vink C, Driessen C, London N, Thijs C, Stobberingh EE. Quantification of Bifidobacterium spp., Escherichia coli and Clostridium difficile in faecal samples of breast-fed and formula-fed infants by real-time PCR. FEMS Microbiol Lett 2005;243:141-7. https://doi.org/10.1016/j.femsle.2004.11.052 https://doi.org/10.1016/j.femsle.2004.11.052
  6. Bezirtzoglou E, Tsiotsias A, Welling GW. Microbiota profile in feces of breast- and formula-fed newborns by using fluorescence in situ hybridization (FISH). Anaerobe 2011;17:478-82. https://doi.org/10.1016/j.anaerobe.2011.03.009 https://doi.org/10.1016/j.anaerobe.2011.03.009
  7. Shan Y, Shan A, Li J, Zhou C. Dietary supplementation of arginine and glutamine enhances the growth and intestinal mucosa development of weaned piglets. Livest Sci 2012;150:369-73. https://doi.org/10.1016/j.livsci.2012.10.006 https://doi.org/10.1016/j.livsci.2012.10.006
  8. Aoyama T, Fukui K, Takamatsu K, Hashimoto Y, Yamamoto T. Soy protein isolate and its hydrolysate reduce body fat of dietary obese rats and genetically obese mice (yellow KK). Nutrition 2000;16:349-54. https://doi.org/10.1016/S0899-9007(00)00230-6 https://doi.org/10.1016/S0899-9007(00)00230-6
  9. Adamson I, Fisher H. Amino acid requirement of the growing rabbit: an estimate of quantitative needs. J Nutr 1973;103:1306-10. https://doi.org/10.1093/jn/103.9.1306 https://doi.org/10.1093/jn/103.9.1306
  10. Farr SA, Banks WA, Kumar VB, Morley JE. Orexin-A-induced feeding is dependent on nitric oxide. Peptides 2005;26:759-65. https://doi.org/10.1016/j.peptides.2004.12.004 https://doi.org/10.1016/j.peptides.2004.12.004
  11. Sheng T, Zhao L, Gao L-F, et al. Lignocellulosic saccharification by a newly isolated bacterium, Ruminiclostridium thermocellum M3 and cellular cellulase activities for high ratio of glucose to cellobiose. Biotechnol Biofuels 2016;9:172. https://doi.org/10.1186/s13068-016-0585-z https://doi.org/10.1186/s13068-016-0585-z
  12. Yutin N, Galperin MY. A genomic update on clostridial phylogeny: gram‐negative spore formers and other misplaced clostridia. Environ Microbiol 2013;15:2631-41. https://doi.org/10.1111/1462-2920.12173
  13. Ahmed I, Abdalla A. Nitrogen and phosphorus fertilization in relation to seed production in onion Allium cepa L. In: VIII African Symposium on Horticultural Crops 143; 1983. pp. 119-26.
  14. Greene JM, Ryan PL. L-arginine in the uterus and placenta and during gestation in mammals. In: L-arginine in clinical nutrition. Cham, Switzerland: Springer (Humana Press); 2017. p. 285-99. https://doi.org/10.1007/978-3-319-26009-9
  15. Sun Y, Chen S, Wei R, et al. Metabolome and gut microbiota variation with long-term intake of Panax ginseng extracts on rats. Food Funct 2018;9:3547-56. https://doi.org/10.1039/C8FO00025E https://doi.org/10.1039/C8FO00025E
  16. Begley M, Gahan CG, Hill C. The interaction between bacteria and bile. FEMS Microbiol Rev 2005;29:625-51. https://doi.org/10.1016/j.femsre.2004.09.003 https://doi.org/10.1016/j.femsre.2004.09.003
  17. Tan B, Li XG, Kong X, et al. Dietary L-arginine supplementation enhances the immune status in early-weaned piglets. Amino Acids 2009;37:323-31. https://doi.org/10.1007/s00726-008-0155-1 https://doi.org/10.1007/s00726-008-0155-1
  18. Awad W, Ghareeb K, Bohm J. Intestinal structure and function of broiler chickens on diets supplemented with a synbiotic containing Enterococcus faecium and oligosaccharides. Int J Mol Sci 2008;9:2205-16. https://doi.org/10.3390/ijms9112205 https://doi.org/10.3390/ijms9112205
  19. Wang K, Liao M, Zhou N, et al. Parabacteroides distasonis alleviates obesity and metabolic dysfunctions via production of succinate and secondary bile acids. Cell Rep 2019;26:222-35. https://doi.org/10.1016/j.celrep.2018.12.028 https://doi.org/10.1016/j.celrep.2018.12.028
  20. Zhang J, Guo Z, Xue Z, et al. A phylo-functional core of gut microbiota in healthy young Chinese cohorts across lifestyles, geography and ethnicities. ISME J 2015;9:1979-90. https://doi.org/10.1038/ismej.2015.11 https://doi.org/10.1038/ismej.2015.11
  21. Pajak B, Orzechowski A, Gajkowska B. Molecular basis of sodium butyrate-dependent proapoptotic activity in cancer cells. Adv Med Sci (De Gruyter Open) 2007;52:83-8.
  22. Ubeda C, Bucci V, Caballero S, et al. Intestinal microbiota containing Barnesiella cures vancomycin-resistant Enterococcus faecium colonization. Infect Immun 2013;8:965-73. http://dx.doi.org/10.1128/IAI.01197-12.
  23. Fiorucci S, Distrutti E. Bile acid-activated receptors, intestinal microbiota, and the treatment of metabolic disorders. Trends Mol Med 2015;21:702-14. https://doi.org/10.1016/j.molmed.2015.09.001
  24. Zinkernagel MS, Zysset-Burri DC, Keller I, et al. Association of the intestinal microbiome with the development of neovascular age-related macular degeneration. Sci Rep 2017;7:40826. https://doi.org/10.1038/srep40826 https://doi.org/10.1038/srep40826
  25. Wu GD, Chen J, Hoffmann C, et al. Linking long-term dietary patterns with gut microbial enterotypes. Science 2011;334:105-8. https://doi.org/10.1126/science.1208344 https://doi.org/10.1126/science.1208344
  26. Mesa D, Lammel DR, Balsanelli E, et al. Cecal microbiota in broilers fed with prebiotics. Front Genet 2017;8:153. https://doi.org/10.3389/fgene.2017.00153 https://doi.org/10.3389/fgene.2017.00153
  27. Huang J, Lin X, Xue B, et al. Impact of polyphenols combined with high-fat diet on rats' gut microbiota. J Funct Foods 2016;26:763-71. https://doi.org/10.1016/j.jff.2016.08.042 https://doi.org/10.1016/j.jff.2016.08.042
  28. Neis EP, Dejong CH, Rensen SS. The role of microbial amino acid metabolism in host metabolism. Nutrients 2015;7:2930-46. https://doi.org/10.3390/nu7042930 https://doi.org/10.3390/nu7042930
  29. Dai Z-L, Li X-L, Xi P-B, Zhang J, Wu G, Zhu W-Y. Regulatory role for L-arginine in the utilization of amino acids by pig small-intestinal bacteria. Amino Acids 2012;43:233-44. https://doi.org/10.1007/s00726-011-1067-z https://doi.org/10.1007/s00726-011-1067-z
  30. Zeng X, Huang Z, Zhang F, Mao X, Zhang S, Qiao S. Oral administration of N-carbamylglutamate might improve growth performance and intestinal function of suckling piglets. Livest Sci 2015;181:242-8. https://doi.org/10.1016/j.livsci.2015.09.004 https://doi.org/10.1016/j.livsci.2015.09.004